Previous Article |
Table of Contents
| Next Article 
Department of Zoology, Göteborg University, Box 463, SE 405 30 Göteborg, Sweden
Edited by Mary Jane West-Eberhard, Smithsonian Tropical Research
Institute, Ciudad Universitaria, Costa Rica, and approved August 22, 2000 (received for review March 28, 2000)
Brood parasitism as an alternative female breeding tactic is
particularly common in ducks, where hosts often receive eggs laid by
parasitic females of the same species and raise their offspring.
Herein, we test several aspects of a kin selection explanation for this
phenomenon in goldeneye ducks (Bucephala clangula) by
using techniques of egg albumen sampling and statistical bandsharing
analysis based on resampling. We find that host and primary parasite
are indeed often related, with mean r = 0.13, about
as high as between first cousins. Relatedness to the host is higher in
nests where a parasite lays several eggs than in those where she lays
only one. Returning young females parasitize their birth nestmates
(social mothers or sisters, which are usually also their genetic
mothers and sisters) more often than expected by chance. Such adult
relatives are also observed together in the field more often than
expected and for longer periods than other females. Relatedness and kin
discrimination, which can be achieved by recognition of birth
nestmates, therefore play a role in these tactics and probably
influence their success.
Alternative breeding tactics,
whereby members of a species differ in the ways they compete over
reproduction, have been discovered in a variety of animals (1). Most
examples concern males, but one widespread such tactic in females is
conspecific brood parasitism, which occurs in some insects, fishes,
amphibia, and birds. It is particularly common in ducks (2). The
parasite lays eggs in the nest of a host female of the same species,
which raises the parasitic as well as her own offspring, probably at a
cost, because she receives no help from the parasite. The parasite can thereby avoid any extra energy cost and predation risk from incubation and rearing of chicks (2). In goldeneyes and some other waterfowl, host
females sometimes prevent a parasite from entering the nest (2).
Female ducks have high return rate to the birth site (natal
philopatry; ref. 3). This return rate makes it likely that some local
females are closely related (mother-daughter or sisters). Propagation
of genes through relatives (4) therefore might favor conspecific brood
parasitism among females in ducks (5, 6) and in certain other birds
where females nest close to their birth site (7, 8). Relatedness
between host and parasite may reduce the fitness cost of being
parasitized for the host (5) or even increase its inclusive fitness
(6), but the role of female philopatry and relatedness in brood
parasitism is still a matter of debate (2, 5-13).
Herein, we test two assumptions of the kin selection hypothesis
(5, 6): (i) host and parasite tend to be related in ducks,
and (ii) this relationship comes about through female natal philopatry and discrimination of close relatives. We use previously unused techniques (14) of nondestructive albumen sampling and protein
fingerprinting of eggs, which greatly help clarify parasitism. Among
902 eggs from 143 female goldeneye ducks (Bucephala
clangula) in 71 nests of a wild population, bandsharing (15) is
higher in the 42 pairs of host and primary parasite than in random
pairs of other females. Additional results show that not only
philopatry, but also kin discrimination through recognition of birth
nestmates, is important in this alternative female breeding tactic.
Ducks are unusual in forming pairs away from the breeding
grounds. The male follows the female to her breeding site, which may be
far from his birth place but near hers (3, 16), making the local
females likely to be related. To test the idea that hosts and parasites
are more closely related than other females, we herein develop protein
bandsharing analysis of electrophoretic albumen bands, produced with
sensitive isoelectric focusing in immobilized pH gradients (14, 17).
Albumen strictly represents the maternal genotype, being secreted by
specific cells in the oviduct (18, 19). Sampling the egg albumen is
therefore like sampling the female directly. Albumen contains more than
a dozen major proteins (18, 20), and genetic polymorphism has been found in many of them; thus, there is considerable genetic variation among females in albumen proteins. Therefore, albumen bands, like DNA
fingerprint bands (e.g., refs. 15 and 21), will reflect differences in
mean relatedness between categories of individuals.
We studied goldeneyes from 1982 to 1997 at Mjörn, a
56-km2 lake 30 km northeast of Göteborg, southwest
Sweden, monitoring up to 125 goldeneye nests. Some nests were in
natural cavities, but the majority were in dispersed nest boxes in
forest trees (on average 120 m from the shore). In a given year,
most parasites laid eggs only parasitically, but several parasites in
addition produced and incubated a clutch of their own (unpublished
work). The present analysis concerns two periods, 1986 and 1988-1991, when albumen was sampled from each of 668 and 234 eggs (59 and 22 nests, respectively), 0-2 days after laying. The samples were stored
at 2°C for 1-5 days, and then kept frozen at After drilling a small hole in the egg, we take a minute albumen
sample (<0.3 ml from a total egg volume of All eggs from a clutch were run on the same gel, and both authors
independently categorized the bands of each egg without knowing its
identity (14). Representatives of all of the different electromorphs
were rerun together on the same gels, with repeats on several gels to
allow direct comparison and estimation of bandsharing across all gels.
An example of a gel is shown in Fig. 1.
Evolution
Host-parasite relatedness shown by protein fingerprinting in a
brood parasitic bird
Abstract
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
Conclusions
Appendix
References
Introduction
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
Conclusions
Appendix
References
Materials and Methods
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
Conclusions
Appendix
References
70°C until the electrophoresis.
60 ml) with a syringe, seal the hole with cyanoacrylate super glue, and return the
egg to the nest; hatchability is preserved (14). The sample is analyzed
electrophoretically, producing a rich pattern of albumen protein bands
with much variation among females. We use isoelectric focusing in
immobilized pH gradients on four different polyacrylamide gels (14). In
isoelectric focusing, proteins are separated in an electric field
applied over a stable pH gradient in the gel. In contrast with the
result of most other electrophoretic methods, each protein therefore
comes to rest as a narrow band at its isoelectric point, where the net
charge of the protein relative to the gel is zero (17). This aspect
greatly facilitates comparison of bands between as well as within gels.
View larger version (121K):
[in a new window]
Fig. 1.
Electrophoretic gel with albumen band patterns for the 12 eggs of
a goldeneye clutch parasitized by three females. There are five host
eggs (lanes marked H) and four, two, and one parasite eggs (lanes
marked 1, 2, and 3, respectively). Bands that were scored for
bandsharing analysis are marked with a short dash in the margin.
Several different bands occur in all 902 eggs and can therefore be used
as location references; they are marked with a longer dash.
Our previous analyses of eggs from 21 individually marked females, identified by video cameras beneath the nest when alighting for egg laying, showed that they had unique albumen band patterns, fully repeatable between years (14). This variation between females, combined with data on laying dates and sites, makes it possible to distinguish the eggs of different females. Among the 21 video-recorded females, 3-14 unique band patterns (differing from each other in one or more bands) emerged per gel type. Combination of the band patterns from all four gel types used made all 21 females distinguishable, because no two females were identical in all bands (14). Other analyses suggest that the resolution of individual identity is similar to that obtained with a DNA multilocus fingerprinting probe; for mother-daughter or sisters, the likelihood that they will have identical albumen banding patterns was estimated at 0.005-0.01 (14).
Video recordings and nest checks at parasitized nests in 1988-1991 showed that the 12 individually marked hosts, which later incubated the clutch, initiated egg laying and produced the highest number of eggs in the nest in all cases but one (ref. 14 and M.Å., unpublished work). For 1986, we therefore assume that the female laying the highest number of eggs was the host. A Monte Carlo simulation based on the numbers of eggs laid by the video-recorded females shows that the risk of mistaking the primary parasite (with more eggs than any other parasite in the nest) for the host is low, about 5.1%. We may have confused host and primary parasite in 1 or 2 of the 29 parasitized nests from 1986 analyzed below; however, this confusion should not influence our estimate of relatedness, because the two females making up the host-parasite pair are still the same. For other than the primary parasite, the risk of confusion with the host is negligibly small, because the other parasites laid so few eggs (unpublished work).
There is no evidence from this or other studies (2) that laying female ducks eliminate eggs not their own.
The present isoelectric focusing method results in a similar number of individually repeatable bands as does multilocus DNA fingerprinting. Albumen is of strictly maternal origin, with band variation that reflects genotypic differences (see above). Therefore, bandsharing analysis, as with DNA fingerprint studies (e.g., 8, 15, 21-24), can be applied to albumen bands for estimating differences in mean relatedness between categories of individuals. For each egg, presence/absence of each band was recorded in a matrix. In total, 98 different bands were found. There was no indication that two females laying in the same nest had identical band patterns (such as two eggs with the same band pattern being laid on the same day in the nest). Removal of 39 bands, each identical in occurrence to another band, resulted in 59 nonredundant bands. The mean number of bands per egg was 11.5 (SD = 1.43). Relatedness is seriously underestimated if common bands are included, and bands with a population frequency >50% should be omitted (15), which reduced the number of bands used to 50.
The bandsharing analysis permits a test of whether host and parasite are closer relatives than other females. We use the bandsharing similarity index Sxy = 2Nxy/(Nx + Ny), where Nxy is the number of bands shared by individuals x and y, and Nx and Ny are the total numbers of bands present in individuals x and y, respectively (e.g., refs. 21-23).
In addition to estimating host-parasite relatedness from eggs, we also tested for possible nestmate recognition and kin discrimination by analyzing the occurrence of marked individuals together on the lake. The hypothesis is that birth nestmates, i.e., the ducklings in the brood and the host female that raises them, may recognize and associate with each other later in life.
Although some of the ducklings are not siblings if the nest has been parasitized, they and the host female will on average be much more closely related than random females. Individual recognition of birth nestmates therefore permits (imperfect) kin discrimination. With the present degree of parasitism, on average about one-third of the chicks are not the genetic offspring of the host, and the mean relatedness between host and chicks is not 0.5 but about 0.4 (see below).
In total, 139 adult females were marked with a unique combination of a numbered steel band and up to three color bands, and 1,172 chicks were marked in the nest with a numbered aluminum tag in each wing. While visiting the study area for trapping females or monitoring broods, we recorded all observations of marked females on the lake. We focused on two frequently visited subareas, each of a size roughly similar to the home range of females (which have an average maximum diameter of 0.52 km; M.Å., unpublished work). We noted whether two marked females were associated: staying or moving together while feeding, preening, or resting, usually less than 5 m from each other (most of the time much closer) and being clearly separated from others during the 15-60 min of observation required to determine the identity of a female. Some pairs of marked females were seen repeatedly over periods of up to several weeks. The time between first and last observation of a pair is used as an estimate of the permanence of their association.
Depending on where they were observed most often, marked females were
assigned to one of the two areas (see Table 2). Several of these
females were known to be birth nestmates. In the list of N
marked females thus obtained for an area, we counted the number of
pairs of nestmates, Nr, that could be
formed. The total number of different pairs that can be formed from
N individuals is NP = N(N 1)/2. We then counted the number,
nm, of different pairs of marked
females that had actually been observed together at least once and
noted how many of these pairs consisted of nestmates, nr. Under the null hypothesis of no
kin discrimination, each possible pair of marked nestmates (in total
Nr pairs) has the same chance of
occurrence as each possible pair of marked nonnestmates
(Np Nr pairs) in the area.
A Monte Carlo test (25, 26) of the null hypothesis was done as follows.
Drawing nm pairs at random from the
altogether Np possible pairs, we
counted the number of pairs drawn that consisted of nestmates. This
count was done for each combination of area and year for which there
were at least two nestmates among the marked birds observed. The total
number of nestmate pairs drawn was counted, and the result was compared
with the actual number of pairs of nestmates
(
nr) observed in the
combined sample for all areas and years (see Table 2). The process was
repeated 105 times. The proportion of cases in
which at least as many pairs of nestmates were drawn as the number
actually observed was calculated, estimating the probability of
obtaining the observed or a more extreme outcome under the null
hypothesis of no nestmate recognition.
| |
Results and Discussion |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
Conclusions
Appendix
References
|
|---|
Host-Parasite Relatedness. If the ratio of gain to loss in inclusive fitness is greater than that for producing an additional own offspring, hosts may gain inclusive fitness by preferentially accepting close relatives as parasites, eliminating costs of parental care for the relative (5, 6). Whatever the costs of being parasitized, which are as yet not sufficiently known, the costs for the host should be more acceptable with increasing relatedness to the parasite. A prediction is therefore that the primary parasite (laying most parasitic eggs) should be related to the host. Lack of relatedness is evidence against the kin selection hypothesis.
The two study periods are first treated separately, then combined. Breeding in 1986 progressed to incubation in 29 parasitized nests (26 of which were parasitized by more than one female), with a mean bandsharing value of 0.288 between host and primary parasite. As the control group, we used the 42 other females sampled in the same area, for which the number of different pairs that can be formed is 42C2 = 42 × 41/2 = 861. We calculated bandsharing for each of these possible pairs and used their mean as the estimate of bandsharing in random pairs of females not involved in host-parasite relationship with each other (15). This mean is 0.163, i.e., 0.125 less than that for host-parasite pairs. The bandsharing distribution is shown in Fig. 2.
|
How Closely Related Are Hosts and Primary Parasites?
Using a regression approach to relatedness, Reeve et al.
(15) derived an estimate of relatedness from DNA fingerprints as
|
[ 1 ] |
0.149. For the
1988-1991 data, the estimate is r = 0.093. The
weighted mean for both periods is r = 0.132, slightly
higher than for first cousins (r = 0.125). This result
does not imply that host-parasite pairs are usually cousins. More
likely, parasites range from being close relatives (mother-daughter or
sisters; see below) to being unrelated to the host. Primary parasites
produced about two-thirds of the parasitic eggs (unpublished work). If
other than primary parasites are also included, the weighted mean
relatedness between host and parasite as expected becomes lower; it is
then estimated at 0.100.
The estimator in Eq. 1 tends to underestimate true
relatedness (15). For this and other reasons, such as the possibility of random misscoring of bands, our estimates are likely to be lower
than the true relatedness.
Kin Discrimination and Favoritism. What is the reason for higher relatedness in host-parasite pairs? One possibility is simply that high return rate of females to the birth site makes close relatives likely to use the same nest site, although they do not recognize each other. Another possibility is that birth nestmates, which are usually close relatives (see below), in addition recognize and treat each other favorably (6, 27, 28). For example, birth nestmates may associate with each other, and hosts may be more tolerant of their birth nestmates than of other parasites. Preferential treatment of adult relatives has rarely been looked for in ducks, but it has been found in female canvasback ducks (Aythya valisineria: ref. 3). Goldeneye broods usually remain together with the host female for at least 5-6 weeks after hatching (29); thus, the chicks and the host may be able to recognize and associate with each other in later years.
The possibility that individual recognition and kin discrimination play a role can be tested in at least two ways. (i) A first prediction is that individual recognition between birth nestmates increases a parasite's ease of access to the nest. A female that lays parasitically in several nests therefore should usually be more closely related to the host for which she lays the most eggs than to the host for which she lays the fewest eggs. This idea can be tested for 20 parasites, each of which laid in several nests. As predicted, host-parasite bandsharing was higher (0.272) in nests where the parasite laid the highest number of eggs (on average 3.0) than where she laid only one egg (0.139; P = 0.018, one-tailed exact permutation test). The mean distance between the two nests was 0.94 km. (Because this test is done within the group of host-parasite pairs, it is statistically independent from the previous test of relatedness, which was done between host-parasite pairs and other females.) (ii) A second prediction is that recognition and relatedness between host and parasite make their interactions peaceful and reduce the risk that the clutch is abandoned or subject to predation. The risk should be higher if there are conspicuous conflicts with unrelated parasites that try to get access to the nest (there is evidence of conflicts in goldeneyes; see ref. 30). Although not significant at the
= 0.05 level, there was a trend in the predicted direction:
bandsharing between host and primary parasite in both periods tended to
be higher among parasitized nests that hatched successfully (1986:
0.347, n = 16; 1988-1991: 0.304, n = 8) than among nests that were abandoned or preyed on during the
incubation period (1986: 0.216, n = 13; 1988-1991:
0.181, n = 5). One-tailed resampled randomization tests
for the two periods gave P = 0.088 and
P = 0.163. Combining these results with Fisher's method (31) gives P = 0.075.
If the previous analysis is expanded to include all parasites laying in
the nests, their weighted mean bandsharing with the host is, for
successful clutches: 0.292 (1986) and 0.297 (1988-1991), and for other
clutches: 0.202 (1986) and 0.184 (1988-1991).
If, as seems likely, host females are not able to distinguish their own
genetic offspring from other chicks in the brood, the average
relatedness between host and chicks in the brood may be of interest in
considerations of inclusive fitness (32, 33). For all of the 35 hatched
clutches studied herein, the weighted mean relatedness between the host
and all chicks in the nest is estimated (from our protein bandsharing
data, with Eq. 1) at 0.399 0.4, as compared with
0.5 for strictly genetic mother-offspring broods. In these
calculations, we assumed that the (unknown) fathers of the chicks were
unrelated to the host female.
Philopatry Effects Only? Can the previous results on host-parasite relatedness be explained simply as consequences of philopatric nest choice not involving individual recognition? Detailed analysis of observed shifts of nest site for marked females suggests that this explanation is unlikely. Even successfully breeding females often shift nest site by over 1 km between years, and returning young females usually breed much farther from the birth nest (on average 0.82 km; n = 16) than required for philopatry to be a sufficient explanation (also see ref. 10). Although our observations of parasitism by marked females are few (n = 6), it has been recorded up to 1.6 km from the birth nest.
For a returning young female, her only substantial chance of parasitizing a close relative through philopatry alone (without individual recognition) is to lay parasitically in the birth nest (Table 1). The earliest females start breeding when 2 years old (mean = 3.1 years; M.Å., unpublished work). For a philopatric 2- to 5-year-old female, estimates from our nesting records show that the probability that one of her birth nestmates is the host in her birth nest is on average only 0.19, if the nest is inhabited (Table 1). (Corresponding estimates of mothers' chances of parasitizing daughters purely through philopatry show that these probabilities are an order of magnitude lower, i.e., negligible.)
|
feeding territory 0.5 km). Video recordings showed that hosts during the laying period usually visit the
nest only every other day, which may allow parasites easy access in
days of host absence. When present, however, the host in 14 of 22 video-recorded cases rose to the entrance hole and prevented the
approaching female from entering (M.Å., unpublished work). In
contrast, only one time in nine did a parasite do so. As expected if
there is discrimination, hosts therefore reject some but not all visits
by other females (also see ref. 2). The females not rejected entered
the nest while the host was present, and in four of these cases, the
parasite laid an egg without any apparent aggression occurring (M.Å.,
unpublished work). Relatedness is, however, not known in most cases,
and a larger sample is needed for meaningful testing of host behavior
in relation to parasite relatedness.
Associations on the Lake Between Birth Nestmates.
We do not know how parasites find the nests of related hosts.
Individual recognition and association on the lake with females from
the birth nest, combined with joint nest visits, is one possibility. Compared with the likelihood of randomly drawing pairs of females that
are birth nestmates from the pool of all marked females present, nestmate pairs are overrepresented in our field observations of marked
pairs (Table 2,
nr). Using these data in a Monte Carlo test of
the null hypothesis of no nestmate or kin discrimination (see
Materials and Methods), we find that the probability of
observing as many as nr = 4 or more different pairs of nestmates is low, P < 0.0038. The null hypothesis is therefore refuted.
|
| |
Conclusions |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
Conclusions
Appendix
References
|
|---|
Genetic relatedness and kin discrimination, which may be achieved indirectly by a combination of natal philopatry and recognition of birth nestmates (or possibly by more sophisticated kin recognition), play a role in conspecific brood parasitism and social behavior in goldeneyes, as previously suggested on theoretical grounds (5, 6). Our preliminary results also suggest that relatedness affects the success of the female alternative reproductive tactics involved, and therefore probably also their frequency. The present findings lead to important questions for research at the interface of reproductive behavior and kin selection, concerning the means and precision by which females discriminate and favor relatives, e.g., at the nest (27, 28); the costs, benefits, and inclusive fitness of the tactics involved (1, 4, 39); and the factors that determine whether a female will be host, parasite, or both (2, 6). The possibility that relatedness plays a role in the evolution of alternative reproductive tactics deserves more attention. Several recent results suggest that relatedness and kin discrimination have even wider importance in animal sociality than anticipated by most researchers except, of course, W. D. Hamilton (4, 27).
| |
Acknowledgements |
|---|
We thank J. Bohlin and U. Unger for help in the field; D. Queller and K. Reeve for helpful discussion; S. Holm for statistical advice; S. Andersson, D. Hasselquist, A. Johnsen, M. Olsson, J. Reynolds, B. Sheldon, T. Slagsvold, H. Smith, the referees, and the editor for constructive suggestions; the Swedish Natural Sciences Research Council for grant support; and E. Bonabeau and the Santa Fe Institute for inviting M.A. to the 1998 workshop on the evolution of social behavior.
| |
Footnotes |
|---|
* To whom reprint requests should be addressed. E-mail: malte.andersson{at}zool.gu.se.
This paper was submitted directly (Track II) to the PNAS office.
See commentary on page 12942.
Article published online before print: Proc. Natl. Acad. Sci. USA, 10.1073/pnas.220137897.
Article and publication date are at www.pnas.org/cgi/doi/10.1073/pnas.220137897
| |
Appendix |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
Conclusions
Appendix
References
|
|---|
For 1986, our approximate bootstrap test (25, 26) of bandsharing
involved sampling with replacement 29 values from the 29 observed
host-parasite bandsharing values, calculating the mean of the sample,
determining whether it is smaller than the mean of the 861 random
control pairs (0.163), and scoring the result if it is smaller. The
process was repeated 106 times, and the total
score was divided by this number to estimate the probability of
obtaining an equally or more extreme result if the null hypothesis were
true. The (one-tailed) outcome for 1986 was P = 0.00267. The corresponding test for the second period, 1988-1991, was
P = 0.1059. These two results from different tests of
the same hypothesis can be combined as suggested by Fisher (31), which
leads to a total probability of P = 0.0026 (
2 test; df = 4; 2 ln
P = 16.34), refuting the null hypothesis.
We also tested the null hypothesis by using a highly conservative randomization test, which resulted in P = 0.045. Our results therefore reject the null hypothesis and corroborate the alternative that host and primary parasite are on average more closely related than females not involved in a host-parasite relationship with each other.
| |
References |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
Conclusions
Appendix
References
|
|---|
| 1. | Gross, M. R. (1996) Trends Ecol. Evol. 11, 92-98. |
| 2. | Sayler, R. D. (1992) in Ecology and Management of Breeding Waterfowl, eds. Batt, B. D. J., Afton, A. D., Anderson, M. G., Ankney, C. D., Johnson, D. H., Kadlec, J. A. & Krapu, G. L. (Univ. of Minnesota Press, Minneapolis), pp. 290-322. |
| 3. | Anderson, M. G. , Rhymer, J. M. & Rohwer, F. C. (1992) in Ecology and Management of Breeding Waterfowl, eds. Batt, B. D. J., Afton, A. D., Anderson, M. G., Ankney, C. D., Johnson, D. H., Kadlec, J. A. & Krapu, G. L. (Univ. of Minnesota Press, Minneapolis), pp. 365-395. |
| 4. | Hamilton, W. D. (1964) J. Theor. Biol. 7, 1-52. |
| 5. | Andersson, M. & Eriksson, M. O. G. (1982) Am. Nat. 120, 1-16. |
| 6. | Andersson, M. (1984) in Producers and Scroungers, ed. Barnard, C. J. (Croom-Helm, London), pp. 195-228. |
| 7. | Emlen, S. T. & Wrege, P. H. (1986) Ethology 71, 2-29. |
| 8. | McRae, S. T. & Burke, T. (1996) Behav. Ecol. Sociobiol. 38, 115-129. |
| 9. | Eadie, J. M. , Kehoe, F. P. & Nudds, T. D. (1988) Can. J. Zool. 66, 1709-1721. |
| 10. | Pöysä, H. , Runko, P. & Ruusila, V. (1997) J. Avian Biol. 28, 63-67. |
| 11. | Weatherhead, P. J. (1998) J. Avian Biol. 29, 321-322. |
| 12. | Zink, A. G. (2000) Am. Nat. 155, 395-405. |
| 13. | Loeb, M. L. G. , Diener, L. M. & Pfennig, D. W. (2000) Anim. Behav. 59, 379-383. |
| 14. | Andersson, M. & Åhlund, M. (2001) Ecology, in press. |
| 15. | Reeve, H. K. , Westneat, D. F. & Queller, D. C. (1992) Mol. Ecol. 1, 223-232. |
| 16. | Greenwood, P. J. & Harvey, P. H. (1982) Annu. Rev. Ecol. Syst. 13, 1-21. |
| 17. | Righetti, P. G. (1990) Immobilized pH Gradients: Theory and Methodology (Elsevier, Amsterdam). |
| 18. | White, H. B. I. (1991) in Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles, eds. Ferguson, M. W. J. & Deeming, D. C. (Cambridge Univ. Press, Cambridge, U.K.), pp. 1-15. |
| 19. | Palmer, B. D. & Guillette, L. J., Jr. (1991) in Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles, eds. Ferguson, M. W. J. & Deeming, D. C. (Cambridge Univ. Press, Cambridge, U.K.), pp. 29-46. |
| 20. | Burley, R. W. & Vadhera, D. V. (1989) The Avian Egg: Chemistry and Biology (Wiley, New York). |
| 21. | Wetton, J. H. , Carter, R. E. , Parkin, D. T. & Walters, D. (1987) Nature (London) 327, 147-149. |
| 22. | Lynch, M. (1990) Mol. Biol. Evol. 7, 478-484. |
| 23. | Danforth, B. B. N. & Freeman-Gallant, C. R. (1996) Mol. Ecol. 5, 221-228. |
| 24. | Birkhead, T. R. , Burke, T. , Zann, R. , Hunter, F. M. & Krupa, A. P. (1990) Behav. Ecol. Sociobiol. 27, 315-324. |
| 25. | Davison, A. C. & Hinkley, D. V. (1997) Bootstrap Methods and Their Application (Cambridge Univ. Press, Cambridge, U.K.). |
| 26. | Manly, F. J. (1997) Randomization, Bootstrap and Monte Carlo Methods in Biology (Chapman & Hall, London) |
| 27. | Hamilton, W. D. (1987) in Kin Recognition in Animals, eds. Fletcher, D. J. C. & Michener, C. D. (Wiley, Chicester, U.K.), pp. 417-438. |
| 28. | Sherman, P. W. , Reeve, H. K. & Pfennig, D. W. (1997) in Behavioural Ecology, eds. Krebs, J. R. & Davies, N. B. (Blackwell, Oxford), pp. 69-96. |
| 29. | Eadie, J. M. , Mallory, M. L. & Lumsden, H. G. (1995) in The Birds of North America, eds. Poole, A. & Gill, F. (Acad. Nat. Sci., Philadelphia), No. 170, pp. 1-32. |
| 30. | Grenquist, P. (1963) Proc. Int. Ornithol. Congr. 13, 685-689. |
| 31. | Sokal, R. R. & Rohlf, F. J. (1995) Biometry (Freeman, New York) |
| 32. | West Eberhard, M. J. (1975) Q. Rev. Biol. 50, 1-33. |
| 33. | Brown, J. L. (1987) Helping and Communal Breeding in Birds (Princeton Univ. Press, Princeton, NJ). |
| 34. | Cooke, F. , Robertson, G. J. & Smith, C. M. (2000) Condor 102, 137-144. |
| 35. | Anderson, M. G. (1985) Ornithol. Monogr. 37, 57-67. |
| 36. | Höglund, J. , Alatalo, R. V. , Lundberg, A. , Rintamäki, P. T. & Lindell, J. (1999) Proc. R. Soc. London Ser. B 266, 813-816. |
| 37. | Pirtney, S. B. , MacColl, A. D. C. , Lambin, X. , Moss, R. & Dallas, J. F. (1999) Biol. J. Linn. Soc. 68, 317-331. |
| 38. | Petrie, M. , Krupa, A. & Burke, T. (1999) Nature (London) 401, 155-157. |
| 39. | Lyon, B. E. (1998) Nature (London) 392, 380-383. |
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg What's this?
Related Commentary in PNAS:
This article has been cited by other articles in HighWire Press-hosted journals:
|
|
 |
|
  P. Waldeck, M. Andersson, M. Kilpi, and M. Ost Spatial relatedness and brood parasitism in a female-philopatric bird population Behav. Ecol., January 1, 2008; 19(1): 67 - 73. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. McKinnon, H. G. Gilchrist, and K. T. Scribner Genetic evidence for kin-based female social structure in common eiders (Somateria mollissima) Behav. Ecol., July 1, 2006; 17(4): 614 - 621. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Poysa Public information and conspecific nest parasitism in goldeneyes: targeting safe nests by parasites Behav. Ecol., May 1, 2006; 17(3): 459 - 465. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. R. Nielsen, B. Semel, P. W. Sherman, D. F. Westneat, and P. G. Parker Host-parasite relatedness in wood ducks: patterns of kinship and parasite success Behav. Ecol., May 1, 2006; 17(3): 491 - 496. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Andersson and J. Wallander Kin selection and reciprocity in flight formation? Behav. Ecol., January 1, 2004; 15(1): 158 - 162. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. P. van der Jeugd, I. T. van der Veen, and K. Larsson Kin clustering in barnacle geese: familiarity or phenotype matching? Behav. Ecol., November 1, 2002; 13(6): 786 - 790. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. D. Sorenson and R. B. Payne Molecular Genetic Perspectives on Avian Brood Parasitism Integr. Comp. Biol., April 1, 2002; 42(2): 388 - 400. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Ruusila, H. Poysa, and P. Runko Costs and benefits of female-biased natal philopatry in the common goldeneye Behav. Ecol., November 1, 2001; 12(6): 686 - 690. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. E. Lyon and J. McA. Eadie Family matters: Kin selection and the evolution of conspecific brood parasitism PNAS, November 21, 2000; 97(24): 12942 - 12944. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||
